Cell-to-cell contact facilitates HIV transmission from lymphocytes to astrocytes via CXCR4

AIDS

Volumn 29, Issue 7, 2015, Pages 755-766

  Li, Guan Han ^a   Anderson, Caroline ^a   Jaeger, Laura ^a   Do, Thao ^b   Major, Eugene O ^a   Nath, Avindra ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

Author keywords

astrocyte; brain; cell to cell transmission; CXCR4; HIV infection; lymphocyte; virological synapse

Indexed keywords

CD4 ANTIBODY; CHEMOKINE RECEPTOR CXCR4; CXCR4 PROTEIN, HUMAN;

ARTICLE; ASTROCYTE; BRAIN; CELL INTERACTION; COCULTURE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; FILOPODIUM; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; LYMPHOCYTE; PRIORITY JOURNAL; SYNAPSE; T LYMPHOCYTE; TRANSMISSION ELECTRON MICROSCOPY; VIRUS ENTRY; VIRUS PARTICLE; VIRUS TRANSMISSION; CELL CULTURE; CELL FUSION; CYTOLOGY; HUMAN IMMUNODEFICIENCY VIRUS; METABOLISM; MICROSCOPY; PHYSIOLOGY; VIROLOGY; VIRUS RELEASE;

ASTROCYTES; CELL FUSION; CELLS, CULTURED; CYTOLOGICAL TECHNIQUES; HIV; HUMANS; LYMPHOCYTES; MICROSCOPY; RECEPTORS, CXCR4; VIRUS INTERNALIZATION; VIRUS RELEASE;

EID: 84928539396     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000000605     Document Type: Article

References (78)

1. Hutter G, Nowak D, Mossner M, Ganepola S, Mussig A, Allers K, et al. Long-term control of HIV by CCR5Delta32/Delta32 stem-cell transplantation. N Engl J Med 2009; 360:692-698.
2. Allers K, Hutter G, Hofmann J, Loddenkemper C, Rieger K, Thiel E, et al. Evidence for the cure of HIV infection by CCR5Delta32/Delta32 stem cell transplantation. Blood 2011; 117:2791-2799.
3. Persaud D, Gay H, Ziemniak C, Chen YH, Piatak M Jr, Chun TW, et al. Absence of detectable HIV-1 viremia after treatment cessation in an infant. N Engl J Med 2013; 369:1828-1835.
4. Tobin NH, Aldrovandi GM. Are infants unique in their ability to be 'functionally cured' of HIV-1 Curr HIV/AIDS Rep 2014; 11:1-10.
5. Kramer-Hammerle S, Rothenaigner I, Wolff H, Bell JE, Brack-Werner R. Cells of the central nervous system as targets and reservoirs of the human immunodeficiency virus. Virus Res 2005; 111:194-213.
6. Churchill M, Nath A. Where does HIV hide? A focus on the central nervous system. Curr Opin HIV AIDS 2013; 8:165-169.
7. Dunfee R, Thomas ER, Gorry PR, Wang J, Ancuta P, Gabuzda D. Mechanisms of HIV-1 neurotropism. Curr HIV Res 2006; 4:267-278.
8. Hickey WF. Basic principles of immunological surveillance of the normal central nervous system. Glia 2001; 36:118-124.
9. Lassmann H, Schmied M, Vass K, Hickey WF. Bone marrow derived elements and resident microglia in brain inflammation. Glia 1993; 7:19-24.
10. McCarthy GF, Leblond CP. Radioautographic evidence for slow astrocyte turnover and modest oligodendrocyte production in the corpus callosum of adult mice infused with 3H-thymidine. J Comp Neurol 1988; 271:589-603.
11. Gavrilin MA, Mathes LE, Podell M. Methamphetamine enhances cell-associated feline immunodeficiency virus replication in astrocytes. J Neurovirol 2002; 8:240-249.
12. Overholser ED, Coleman GD, Bennett JL, Casaday RJ, Zink MC, Barber SA, et al. Expression of simian immunodeficiency virus (SIV) nef in astrocytes during acute and terminal infection and requirement of nef for optimal replication of neurovirulent SIV in vitro. J Virol 2003; 77:6855-6866.
13. Thompson KA, Varrone JJ, Jankovic-Karasoulos T, Wesselingh SL, McLean CA. Cell-specific temporal infection of the brain in a simian immunodeficiency virus model of human immunodeficiency virus encephalitis. J Neurovirol 2009; 15:300-311.
14. Tornatore C, Nath A, Amemiya K, Major EO. Persistent human immunodeficiency virus type 1 infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J Virol 1991; 65:6094-6100.
15. Sabri F, Tresoldi E, Di Stefano M, Polo S, Monaco MC, Verani A, et al. Nonproductive human immunodeficiency virus type 1 infection of human fetal astrocytes: independence from CD4 and major chemokine receptors. Virology 1999; 264:370-384.
16. Chauhan A, Mehla R, Vijayakumar TS, Handy I. Endocytosismediated HIV-1 entry and its significance in the elusive behavior of the virus in astrocytes. Virology 2014; 456-457:1-19.
17. Maldarelli F,WuX, Su L, Simonetti FR, Shao W, Hill S, et al. HIV latency. Specific HIV integration sites are linked to clonal expansion and persistence of infected cells. Science 2014; 345:179-183.
18. Tornatore C, Chandra R, Berger JR, Major EO. HIV-1 infection of subcortical astrocytes in the pediatric central nervous system. Neurology 1994; 44:481-487.
19. Ranki A, Nyberg M, Ovod V, Haltia M, Elovaara I, Raininko R, et al. Abundant expression of HIV Nef and Rev proteins in brain astrocytes in vivo is associated with dementia. AIDS 1995; 9:1001-1008.
20. Takahashi K, Wesselingh SL, Griffin DE, McArthur JC, Johnson RT, Glass JD. Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann Neurol 1996; 39:705-711.
21. An SF, Groves M, Gray F, Scaravilli F. Early entry and widespread cellular involvement of HIV-1 DNA in brains of HIV-1 positive asymptomatic individuals. J Neuropathol Exp Neurol 1999; 58:1156-1162.
22. Anderson CE, Tomlinson GS, Pauly B, Brannan FW, Chiswick A, Brack-Werner R, et al. Relationship of Nef-positive and GFAPreactive astrocytes to drug use in early and late HIV infection. Neuropathol Appl Neurobiol 2003; 29:378-388.
23. McCarthy M, He J, Wood C. HIV-1 strain-associated variability in infection of primary neuroglia. J Neurovirol 1998; 4:80-89.
24. Di Rienzo AM, Aloisi F, Santarcangelo AC, Palladino C, Olivetta E, Genovese D, et al. Virological and molecular parameters of HIV-1 infection of human embryonic astrocytes. Arch Virol 1998; 143:1599-1615.
25. Vijaykumar TS, Nath A, Chauhan A. Chloroquine mediated molecular tuning of astrocytes for enhanced permissiveness to HIV infection. Virology 2008; 381:1-5.
26. Churchill MJ, Wesselingh SL, Cowley D, Pardo CA, McArthur JC, Brew BJ, et al. Extensive astrocyte infection is prominent in human immunodeficiency virus-associated dementia. Ann Neurol 2009; 66:253-258.
27. Levy DN, Aldrovandi GM, Kutsch O, Shaw GM. Dynamics of HIV-1 recombination in its natural target cells. Proc Natl Acad Sci U S A 2004; 101:4204-4209.
28. Brown A, Gartner S, Kawano T, Benoit N, Cheng-Mayer C. HLAA2 down-regulation on primary human macrophages infected with an M-tropic EGFP-tagged HIV-1 reporter virus. J Leukoc Biol 2005; 78:675-685.
29. Nuovo GJ, Gallery F, MacConnell P, Braun A. In situ detection of polymerase chain reaction-amplified HIV-1 nucleic acids and tumor necrosis factor-alpha RNA in the central nervous system. Am J Pathol 1994; 144:659-666.
30. Ma M, Geiger JD, Nath A. Characterization of a novel binding site for the human immunodeficiency virus type 1 envelope protein gp120 on human fetal astrocytes. J Virol 1994; 68:6824-6828.
31. Peudenier S, Hery C, Ng KH, Tardieu M. HIV receptors within the brain: A study of CD4 and MHC-II on human neurons, astrocytes and microglial cells. Res Virol 1991; 142:145-149.
32. Dewhurst S, Sakai K, Bresser J, Stevenson M, Evinger-Hodges MJ, Volsky DJ. Persistent productive infection of human glial cells by human immunodeficiency virus (HIV) and by infectious molecular clones of HIV. J Virol 1987; 61:3774-3782.
33. Shahabuddin M, Volsky B, Kim H, Sakai K, Volsky DJ. Regulated expression of human immunodeficiency virus type 1 in human glial cells: induction of dormant virus. Pathobiology 1992; 60:195-205.
34. Canki M, Thai JN, Chao W, Ghorpade A, Potash MJ, Volsky DJ. Highly productive infection with pseudotyped human immunodeficiency virus type 1 (HIV-1) indicates no intracellular restrictions to HIV-1 replication in primary human astrocytes. J Virol 2001; 75:7925-7933.
35. Brack-Werner R, Kleinschmidt A, Ludvigsen A, Mellert W, Neumann M, Herrmann R, et al. Infection of human brain cells by HIV-1: restricted virus production in chronically infected human glial cell lines. AIDS 1992; 6:273-285.
36. Nath A, Hartloper V, Furer M, Fowke KR. Infection of human fetal astrocytes with HIV-1: viral tropism and the role of cell to cell contact in viral transmission. J Neuropathol Exp Neurol 1995; 54:320-330.
37. Dimitrov DS, Willey RL, Sato H, Chang LJ, Blumenthal R, Martin MA. Quantitation of human immunodeficiency virus type 1 infection kinetics. J Virol 1993; 67:2182-2190.
38. Sourisseau M, Sol-Foulon N, Porrot F, Blanchet F, Schwartz O. Inefficient human immunodeficiency virus replication in mobile lymphocytes. J Virol 2007; 81:1000-1012.
39. Chen P, Hubner W, Spinelli MA, Chen BK. Predominant mode of human immunodeficiency virus transfer between T cells is mediated by sustained Env-dependent neutralization-resistant virological synapses. J Virol 2007; 81:12582-12595.
40. Jolly C, Mitar I, Sattentau QJ. Adhesion molecule interactions facilitate human immunodeficiency virus type 1-induced virological synapse formation between T cells. J Virol 2007; 81:13916-13921.
41. Rudnicka D, Feldmann J, Porrot F, Wietgrefe S, Guadagnini S, Prevost MC, et al. Simultaneous cell-to-cell transmission of human immunodeficiency virus to multiple targets through polysynapses. J Virol 2009; 83:6234-6246.
42. Hubner W, McNerney GP, Chen P, Dale BM, Gordon RE, Chuang FY, et al. Quantitative 3D video microscopy of HIV transfer across T cell virological synapses. Science 2009; 323:1743-1747.
43. Felts RL, Narayan K, Estes JD, Shi D, Trubey CM, Fu J, et al. 3D visualization of HIV transfer at the virological synapse between dendritic cells and T cells. Proc Natl Acad Sci U S A 2010; 107:13336-13341.
44. Do T, Murphy G, Earl LA, Del Prete GQ, Grandinetti G, Li GH, et al. Three-dimensional imaging of HIV-1 virological synapses reveals membrane architectures involved in virus transmission. J Virol 2014; 88:10327-10339.
45. Rezaie P, Trillo-Pazos G, Everall IP, Male DK. Expression of beta-chemokines and chemokine receptors in human fetal astrocyte and microglial co-cultures: potential role of chemokines in the developing CNS. Glia 2002; 37:64-75.
46. Harouse JM, Bhat S, Spitalnik SL, Laughlin M, Stefano K, Silberberg DH, et al. Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide. Science 1991; 253:320-323.
47. Hao HN, Lyman WD. HIV infection of fetal human astrocytes: The potential role of a receptor-mediated endocytic pathway. Brain Res 1999; 823:24-32.
48. Liu Y, Liu H, Kim BO, Gattone VH, Li J, Nath A, et al. CD4-independent infection of astrocytes by human immunodeficiency virus type 1: requirement for the human mannose receptor. J Virol 2004; 78:4120-4133.
49. Deiva K, Khiati A, Hery C, Salim H, Leclerc P, Horellou P, et al. CCR5-, DC-SIGN-dependent endocytosis and delayed reverse transcription after human immunodeficiency virus type 1 infection in human astrocytes. AIDS Res Hum Retroviruses 2006; 22:1152-1161.
50. Joyner AS, Willis JR, Crowe JE Jr, Aiken C. Maturation-induced cloaking of neutralization epitopes on HIV-1 particles. PLoS Pathog 2011; 7:e1002234.
51. WymaDJ, Kotov A, Aiken C. Evidence for a stable interaction of gp41 with Pr55(Gag) in immature human immunodeficiency virus type 1 particles. J Virol 2000; 74:9381-9387.
52. Murakami T, Ablan S, Freed EO, Tanaka Y. Regulation of human immunodeficiency virus type 1 Env-mediated membrane fusion by viral protease activity. J Virol 2004; 78:1026-1031.
53. Pang HB, Hevroni L, Kol N, Eckert DM, Tsvitov M, Kay MS, et al. Virion stiffness regulates immature HIV-1 entry. Retrovirology 2013; 10:4.
54. Berson JF, Doms RW. Structure-function studies of the HIV-1 coreceptors. Semin Immunol 1998; 10:237-248.
55. Zhuang K, Leda AR, Tsai L, Knight H, Harbison C, Gettie A, et al. Emergence of CD4 independence envelopes and astrocyte infection in R5 simian-human immunodeficiency virus model of encephalitis. J Virol 2014; 88:8407-8420.
56. Croitoru-Lamoury J, Guillemin GJ, Boussin FD, Mognetti B, Gigout LI, Cheret A, et al. Expression of chemokines and their receptors in human and simian astrocytes: evidence for a central role of TNF alpha and IFN gamma in CXCR4 and CCR5 modulation. Glia 2003; 41:354-370.
57. Gabuzda D, Wang J. Chemokine receptors and mechanisms of cell death in HIV neuropathogenesis. J Neurovirol 2000; 6 (Suppl 1):S24-S32.
58. Yao H, Bethel-Brown C, Li CZ, Buch SJ. HIV neuropathogenesis: A tight rope walk of innate immunity. J Neuroimmune Pharmacol 2010; 5:489-495.
59. Shapshak P, Duncan R, Minagar A, Rodriguez de la Vega P, Stewart RV, Goodkin K. Elevated expression of IFN-gamma in the HIV-1 infected brain. Front Biosci 2004; 9:1073-1081.
60. Weinberger AD, Perelson AS. Persistence and emergence of X4 virus in HIV infection. Math Biosci Eng 2011; 8:605-626.
61. Peters PJ, Duenas-Decamp MJ, Sullivan WM, Brown R, Ankghuambom C, Luzuriaga K, et al. Variation in HIV-1 R5 macrophage-tropism correlates with sensitivity to reagents that block envelope: CD4 interactions but not with sensitivity to other entry inhibitors. Retrovirology 2008; 5:5.
62. Ohagen A, Devitt A, Kunstman KJ, Gorry PR, Rose PP, Korber B, et al. Genetic and functional analysis of full-length human immunodeficiency virus type 1 env genes derived from brain and blood of patients with AIDS. J Virol 2003; 77:12336-12345.
63. Gorry PR, Bristol G, Zack JA, Ritola K, Swanstrom R, Birch CJ, et al. Macrophage tropism of human immunodeficiency virus type 1 isolates from brain and lymphoid tissues predicts neurotropism independent of coreceptor specificity. J Virol 2001; 75:10073-10089.
64. Spudich SS, Huang W, Nilsson AC, Petropoulos CJ, Liegler TJ, Whitcomb JM, et al. HIV-1 chemokine coreceptor utilization in paired cerebrospinal fluid and plasma samples: A survey of subjects with viremia. J Infect Dis 2005; 191:890-898.
65. Buch S, Sui Y, Dhillon N, Potula R, Zien C, Pinson D, et al. Investigations on four host response factors whose expression is enhanced in X4 SHIV encephalitis. J Neuroimmunol 2004; 157:71-80.
66. Vissers M, Stelma FF, Koopmans PP. Could differential virological characteristics account for ongoing viral replication and insidious damage of the brain during HIV 1 infection of the central nervous system? J Clin Virol 2010; 49:231-238.
67. Speck RF, Esser U, Penn ML, Eckstein DA, Pulliam L, Chan SY, et al. A trans-receptor mechanism for infection of CD4-negative cells by human immunodeficiency virus type 1. Curr Biol 1999; 9:547-550.
68. Boutet A, Salim H, Taoufik Y, Lledo PM, Vincent JD, Delfraissy JF, et al. Isolated human astrocytes are not susceptible to infection by M-and T-tropic HIV-1 strains despite functional expression of the chemokine receptors CCR5 and CXCR4. Glia 2001; 34:165-177.
69. Lee SJ, Benveniste EN. Adhesion molecule expression and regulation on cells of the central nervous system. J Neuroimmunol 1999; 98:77-88.
70. Dietrich JB. The adhesion molecule ICAM-1 and its regulation in relation with the blood-brain barrier. J Neuroimmunol 2002; 128:58-68.
71. Petito CK, Adkins B, McCarthy M, Roberts B, Khamis I. CD4R and CD8R cells accumulate in the brains of acquired immunodeficiency syndrome patients with human immunodeficiency virus encephalitis. J Neurovirol 2003; 9:36-44.
72. Kibayashi K, Mastri AR, Hirsch CS. Neuropathology of human immunodeficiency virus infection at different disease stages. Hum Pathol 1996; 27:637-642.
73. Czub S, Muller JG, Czub M, Muller-Hermelink HK. Nature and sequence of simian immunodeficiency virus-induced central nervous system lesions: A kinetic study. Acta Neuropathol 1996; 92:487-498.
74. Ryan G, Grimes T, Brankin B, Mabruk MJ, Hosie MJ, Jarrett O, et al. Neuropathology associated with feline immunodeficiency virus infection highlights prominent lymphocyte trafficking through both the blood-brain and blood-choroid plexus barriers. J Neurovirol 2005; 11:337-345.
75. Peng H, Erdmann N, Whitney N, Dou H, Gorantla S, Gendelman HE, et al. HIV-1-infected and/or immune activated macrophages regulate astrocyte SDF-1 production through IL-1beta. Glia 2006; 54:619-629.
76. Hesselgesser J, Horuk R. Chemokine and chemokine receptor expression in the central nervous system. J Neurovirol 1999; 5:13-26.
77. Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci U S A 1986; 83:7089-7093.
78. Willey SJ, Reeves JD, Hudson R, Miyake K, Dejucq N, Schols D, et al. Identification of a subset of human immunodeficiency virus type1(HIV-1),HIV-2,andsimianimmunodeficiencyvirusstrains able to exploit an alternative coreceptor on untransformed human brain and lymphoid cells. J Virol 2003; 77:6138-6152.